A New Species of Utricularia (Lentibulariaceae) from Chapada

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A New Species of Utricularia (Lentibulariaceae) from Chapada dos Veadeiros (Central Brazil) Author(s): Paulo Cesar Baleeiro Souza and Claudia Petean Bove Source: Systematic Botany, 36(2):465-469. 2011. Published By: The American Society of Plant Taxonomists URL: http://www.bioone.org/doi/full/10.1600/036364411X569642

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Systematic Botany (2011), 36(2): pp. 465–469 © Copyright 2011 by the American Society of Plant Taxonomists DOI 10.1600/036364411X569642 A New Species of Utricularia (Lentibulariaceae) from Chapada dos Veadeiros (Central Brazil)

Paulo Cesar Baleeiro Souza1, 2 and Claudia Petean Bove1 1 Laboratório de Plantas Aquáticas, Departamento de Botânica, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, Rio de Janeiro 20940-040, Brazil 2 Author for correspondence ( [email protected] )

Communicating Editor: Kenneth M. Cameron

Abstract— A new species, Utricularia densiflora , from the Brazilian savanna (Cerrado) is described and illustrated. This species was found growing at the Chapada dos Veadeiros National Park, and is distinguished from the other species in the genus by the presence of several rudimentary (or dormant) floral buds, sessile glands in the peduncle, and highly congested inflorescence. Utricularia densiflora is here considered a member of section Oligocista and is morphologically similar to U. erectiflora and U. meyeri. A key of the Utricularia species inhabiting the Chapada dos Veadeiros National Park is provided.

Resumo—Uma nova espécie, Utricularia densiflora , do Cerrado brasileiro é descrita e ilustrada. Essa espécie foi encontrada no Parque Nacional da Chapada dos Veadeiros. Distingue-se das demais espécies do gênero pela presença de muitos botões florais rudimentares (ou dormentes), glândulas sésseis no pedúnculo e inflorescência altamente congesta. Utricularia densiflora é aqui considerada membro da seção Oligocista e morfologicamente semelhante à U. erectiflora e U. meyeri . É disponibilizada uma chave de identificação das espécies ocorrentes no Parque Nacional da Chapada dos Veadeiros. Keywords— aquatic plant , Brazil , Cerrado , Chapada dos Veadeiros , new species , taxonomy.

Utricularia L. is the largest genus of Lentibulariaceae and all light microscope (LM) with capture system composed by camera Q, carnivorous plants, with species distributed worldwide and color 5 and software Image Pro-Express. The seed surface was air- dried, mounted and coated with a gold-palladium (40–60%), and then diversified in tropical regions ( Taylor 1989 ; Jobson et al. 2003 ; observed using a Jeol JSM 6390 LV Scanning Electron Microscope Müller and Borsch 2005 ; Guisande et al. 2007 ). According to (SEM); both process at the Museu Nacional do Rio de Janeiro (UFRJ), the Brazilian species list of Lentibulariaceae undertaken by Brazil. Miranda and Rivadavia (2010), Utricularia is represented by 67 species, distributed among various biomes, ca. 48 species Taxonomic Treatment occurring in the Brazilian Cerrado vegetation. Since Taylor’s Utricularia densiflora Baleeiro & C. P. Bove, sp. nov.—TYPE: monograph (1989), a single new species, U. cochleata C. P. BRAZIL. Goiás: Município de Alto Paraíso de Goiás, Bove, has been described for this domain (Bove 2008). The Parque Nacional Chapada dos Veadeiros, Serra da Baleia, Cerrado is a hotspot for conservation due to its great biologi- 1,100 m, 3 Jun 2009, P. C. Baleeiro 21, C. P. Bove 2020, cal diversity and high endemic index (ca. 44% of the species), A. L. R. Oliveira & R. Couto (hototype: R!; isotypes: K!, but unfortunately it has lost about 55% of their original terri- SPF!). tory due to human impacts (Klink and Machado 2005), with only small areas under protection, such as the Chapada dos Hidrostadia herbacea. Utriculi foliis, stolonibus, ramis et Veadeiros National Park (State of Goiás), created in 1961 and rhizoideis. Inflorescentia erecta, satis congesta, scapo variis which has been recognized by UNESCO as a World Natural glandulis essilibus, racemo ca. 15 floribus flavis, ca. 5 mm Heritage Site since December 2001. This Park is a high- longis; ca. 20 alabastris abortivis subintelectis unusquodque land complex of 65,514 ha with altitudes ranging from 500– bractea, inflorescentiae mox infra. 1,650 m ( Munhoz and Felfili 2006 ). The region is composed Hydrophytic herb. Rhizoids few or many 2–6, from the by many diverse habitats, such as open fields (grasslands) base of the peduncle, filiform, 5–32 × 0.2–0.4 mm, bearing and swampy areas near streams lined with the palm tree papillose branches up to 8 mm long, sometimes branched. Mauritia flexuosa L. f., a habitat known regionally as “vere- Stolons numerous, filiform, branched, up to 8 cm long, ca. das.” While undertaking a floristic survey of Utricularia in 0.2 mm thick. Leaves from the stolons, peduncle base and the Cerrado, a new Utricularia species was found and is here rhizoids, petiolate, lamina linear to narrowly obovate, apex described. rounded, 1-nerved; up to 18 × 1 mm. Traps numerous on the leaves, stolons, stolon branches, rhizoids and rhiz- Materials and Methods oid branches, globose, sometimes with a prominent ventral, chin-like swelling, ca. 1 mm long, subsessile or stalked, The type specimen described below is deposited as spirit in R, mouth basal with double, conical, dorsal appendages, outer SPF and K (acronyms after Thiers 2010 ). General morphology and measurements were undertaken with a stereoscope and light micro- surface of the trap papillose, trap interior with bifid glands. scope. A paradermic section of the peduncle was done for sessile Inflorescence with spirally arranged bracts and flowers, ca. glands visualization. The image was obtained by a Olympus BX – 51 10 cm long. Peduncle sometimes sparsely branched below,

465 466 SYSTEMATIC BOTANY [Volume 36 terete, 1 mm thick, bearing numerous sessile glands densely Conservation Status—According to the IUCN (IUCN 2001) concentrated near the base. Scales ca. 3, ovate, apex acute, U. densiflora is here classified as Near Threatened (NT). 0.6–1.0 × 0.3–0.5 mm. Rudimentary (or dormant) buds below the lowermost opened flower, (7–)15–23 congested above Discussion and becoming lax towards peduncle base. Bracts strongly convex, margins curved inwards, broadly ovate with apex Oligocista A. DC. is the largest section in the genus Utricularia acute or acuminate, 1.8 × 1.5 mm. Bracteoles linear, 0.7 × 0.2 (37 species), but only a few species occur in the neotropics (six mm. Calyx lobes unequal, ovate, upper lobe 2.0 × 1.0 mm, species). Utricularia densiflora is here considered a member of apex rounded, lower lobe 1.8 × 1.2 mm, apex acute. Corolla this section, due to its galeate lower lip corolla, divergent pale yellow, 0.5 mm long. Filaments almost straight, 0.6 mm spur, calyx lobes subsimilar enclosing the capsule, external long, anther thecae distinct, 0.3 mm long. Ovary globose, morphology and internal glands of the traps, and pollen mor- 0.4 mm long, style very minute, stigma lower lip semicir- phology. Additional features include simple leaves, basifixed cular, upper lip inconspicuous. Flowers 5–16, located above relatively broad bracts, bracteoles present, and seed morphol- the rudimentary buds, densely congested, pedicel erect, fili- ogy ( Fig. 2B ). Utricularia densiflora is morphologically most form, 1.7 mm long. Bracts basifixed, ovate to widely ovate, similar to U. erectiflora and U. meyeri due to the upper corolla with apex acute 1.5–3 × 1–2 mm. Bracteoles lanceolate to nar- lobe shape, involute calyx margin, with decurrent base, and rowly ovate, ca. 1.0 × 0.4 mm. Calyx lobes subsimilar, decur- narrow leaf lamina with rounded apex. The lower corolla lobe rent at the base, green with winy apex, accrescent enclosing of U. densiflora resembles that of U. meyeri, which has less con- the capsule, margins strongly involute, obscurely nerved; gested inflorescences. Utricularia densiflora is unique in having lower lobe ovate, apex obtuse, 3 × 2.3 mm, upper lobe widely rudimentary buds subtended by bracts along the peduncle; ovate with apex acute or acuminate, 3 × 3 mm. Corolla yel- strongly congested raceme, numerous sessile glands near the low, 3–5 mm long; upper lip oblong, constricted near the peduncle base (Fig. 2A) becoming scarce towards the apex; center, apex rounded or slightly truncate, entire; lower lip spur as long as the lower calyx lobe and rhizoid branches galeate, approximately circular in outline, slightly swol- somewhat ramified ( Table 1 ). len near the base, entire or emarginated apex. Palate with The rhizoids in Utricularia densiflora are the biggest of the a raised, microscopically ciliate rim. Spur subulate, curved section (up to 3.5 cm long while those of U. meyeri Pilg. are upwards, with acute apex as long as the lower calyx lobe. up to 2 cm long); interestingly, these rhizoids branch pro- Filaments almost straight, 1.1 mm long, anther thecae dis- fusely, a rare feature in the genus. In section Oligocista branch- tinct, 0.8 mm long. Pollen 4–5-colporate. Ovary globose; ing rhizoids are only seen to a lesser degree in U. letestui style short; stigma bilabiate, lower lip semicircular, recurved, P. Taylor ( Taylor 1989 ). Presumably the size of the rhizoids upper lip similar but smaller. Capsule globose, glabrous, up and the number of branches enhance the anchoring function to 2.3 mm. Seeds broadly ovoid, 0.25–1.0 mm long, testa retic- of the relatively large inflorescences of U. densiflora in its shal- ulate, testa cells elongated with boundaries raised, straight low water habitat. to somewhat sinuate, slightly granulose, large lumina The rudimentary buds resemble large scales at first longitudinally striate with bridges connecting the stria glance (Fig. 1A). The bracts are wider than the calyx lobes, beneath. although somewhat shorter, bearing a minute corolla, gynoe- Etymology— From the Latin densus (a, um) plus flora, in cium, and androecium. Taylor (1989:18) mentioned just one reference to the extremely congested flowers on the inflores- rudimentary bud in several species of section Pleiochasia cence ( Fig. 1A ). (Kamien´ski) Barnhart, U. simplex R. Br. in section Australes Geographic Distribution and Ecology— Although exten- P. Taylor and U. warmingii Kamien´ski in section Utricularia sive field work was carried out at the Chapada dos Veadeiros, P. Taylor. The single rudimentary buds described by Taylor as well as careful examination of Utricularia collections from are rare occurrences in the species cited, which was not central Brazil (CEN, HEPH, HMS, IBGE, NX, UB, UFG, R, mentioned by him in the specific detailed descriptions. RB, SP and SPF), U. densiflora is thus far only known from one All U. densiflora inflorescences studied at the type popula- locality, near the Serra da Baleia, located within the Chapada tion presented numerous rudimentary buds, thus clearly an dos Veadeiros National Park, Goiás state. Utricularia den- autapomorphy. siflora occurs sympatrically with Eriocaulon aff. heteropep- Twenty two species of Utricularia have been recorded for lon Silveira in natural pools of water ca. 7 cm deep among Chapada dos Veadeiros National Park (P. C. Baleeiro, pers. grasslands. obs.). An identification key for this region is provided below. 2011] BALEEIRO AND BOVE: NEW SPECIES OF UTRICULARIA 467

F ig . 1. Utricularia densiflora. A – B. Habit. A. Apex of plant with raceme and rudimentary buds. B. Base of plant with scales and peduncle base with: B1 – rhizoids, B2 – stolon and stolon branches, B3 - leaf and traps. C. Trap detail. D. Aerial inflorescence view. E. Rudimentary bud lateral view. F. Rudimentary bud longitudinal section. G. Bract. H. Bracteoles. I. Flower with bract and bracteoles. J. Corolla lateral view. K. Corolla upper lobe. L. Calyx. M. Pistil and stamens. N. Calyx enclosing the young capsule. (P. C. Baleeiro 21 et al. ). 468 SYSTEMATIC BOTANY [Volume 36

F ig . 2. Utricularia densiflora . A. LM of peduncle base showing the sessile glands (white arrow in one of them). B. SEM of seed.

Key to Species of UTRICULARIA from Chapada dos Veadeiros, Goiás State, Brazil 1. Bracts basisolute ...... 2 2. Bracteoles present ...... U. pubescens 2. Bracteoles absent ...... 3 3. Corolla yellow ...... 4 4. Spur of corolla twice as long as the lower lip ...... U. nigrescens 4. Spur of corolla as long as the lower lip or smaller ...... 5 5. Nerves of calyx lobes obscure or absent ...... U. trichophylla 5. Nerves of calyx lobes prominent or distinct ...... 6 6. Nerves of calyx prominent, extending to the rounded apex ...... U. triloba 6. Nerves of calyx distinct, not extending to the rounded apex ...... U. subulata 3. Corolla violet or white ...... 7 7. Leaves divided into capillary segments ...... U. neottioides 7. Leaves not divided into capillary segments ...... 8 8. Trap mouth with a single ventral appendage ...... U. cucullata 8. Trap mouth with no appendage ...... U. myriocista 1. Bracts basifixed ...... 9 9. Bracteoles and scales absent ...... 10 10. Peduncle distinct, ca. 2 mm long, bract boat-shaped, hyaline ...... U. biovularioides 10. Peduncle extremely short, ca. 0.5 mm long or apparently absent, bract transversally oblong, not hyaline ...... U. olivacea 9. Bracteoles and scales present ...... 11 11. Corolla yellow ...... 12 12. Bracts, bracteoles and scales margins fimbriate-dentate ...... U. simulans 12. Bracts, bracteoles or scales margins laciniate or entire ...... 13 13. Leaves dimorphic, corolla 1.5–2.0 cm long ...... U. praelonga 13. Leaves not dimorphic, corolla up to 1.0 cm long ...... 14 14. Spur conical, wider than long ...... U. guyanensis 14. Spur subulate, much longer than wide ...... 15 15. Traps without appendages, long stalked, upper calyx lobe with prominently raised nerves ...... U. nana 15. Traps with two dorsal appendages, stalked or sessile, upper calyx lobe without prominently raised nerves ...... 16 16. Dormant buds present on the peduncle, pedicel about half as long as the calyx ...... U. densiflora 16. No dormant buds on the peduncle, pedicel about as long as the calyx ...... U. laxa 11. Corolla violet or white ...... 17 17. Bracts and bracteoles basally connate ...... 18 18. Lower corolla lip ca. 2 cm wide, not lobed or very shallowly 3- lobed ...... U. tricolor 18. Lower corolla lip 0.25–1 cm wide, distinctly 3-lobed ...... U. amethystina 17. Bracts and bracteoles not basally connate ...... 19 19. Calyx with raised, prominent nerves ...... U. purpureocaerulea 19. Calyx nerves not prominent or raised ...... 20 20. Capsule narrowly ellipsoid to very narrowly ovoid ...... U. tenuissima 20. Capsule globose ...... 21 21. Lower corolla lip 4-lobed and upper lip 2-lobed ...... U. laciniata 21. Lower corolla lip slightly 3-lobed and upper lip entire ...... U. hispida 2011] BALEEIRO AND BOVE: NEW SPECIES OF UTRICULARIA 469

Table 1. Comparative diagnostic characters among Utricularia densiflora , U. erectiflora, and U. meyeri .

U. densiflora U. erectiflora U. meyeri Rhizoids Few to numerous Few Numerous Peduncle and stolon With several sessile glands Glabrous Glabrous Leaves Few from the peduncle base and None from the peduncle and None from the peduncle and few numerous from the stolons numerous from the stolons from the stolons Traps Numerous on the leaves, stolons and Occasionally on leaves, numerous on Few on the stolons and rhizoids stolon branches, few on rhizoids the stolons, apparently absent from rhizoids Bracteoles Shorter than the bract. Lanceolate to As long as the bract. Linear Slightly shorter than the bract. Linear narrowly ovate Bracts with rudimentary (7-)15–23 None None (or dormant) floral buds Corolla 3–5 mm 8–12 mm 15–20 mm Calyx lower lobe apex Entire, reddish Shortly bifid, green Shortly bifid, green Relationship between spur and lower calyx lobe Equal in length 2 times longer 3–4 times longer

Acknowledgments. This research was carried out with financial sup- Jobson, R. W., J. Playford , K. M. Cameron , and V. A. Albert . 2003 . Molecular port of Postgraduate Program in Biological Sciences (Botany) – National phylogenetics of Lentibulariaceae inferred from plastid rps16 intron Museum of Universidade Federal do Rio de Janeiro and Conselho and trnL-F DNA sequences: implications for character evolution and Nacional de Pesquisa e Desenvolvimento- CNPq (grant to P. C. Baleeiro). biogeography . Systematic Botany 28: 157 – 171 . We thank Dr. Pedro Carauta for the Latin diagnosis, Dr. Gabriel Bernadello Klink, C. A. and R. B. Machado . 2005 . Conservation of the Brazilian for suggestions on the manuscript, Fernando Rivadavia for English revi- Cerrado . Conservation Biology 19: 707 – 713 . sion, Ricardo Moura for aid in choosing the plant name, Adriana Oliveira Miranda, V. F. O. and F. Rivadavia . 2010 . Lentibulariaceae . Pp 1163 – 1166 for the Eriocaulon identification and for aiding Figure 2 organization. in Catálogo de Plantas e Fungos do Brasil , vol. 2 , eds. R. C. Forza ; J. F. A. Fieldwork could not have been conducted without the valuable assistance Baumgratz ; C. E. M. Bicudo ; A. A. Carvalho-Jr .; A. Costa ; D. P. Costa ; of Adriana Oliveira and Ricardo Couto. We also thank SISBIO/IBAMA M. Hopkins ; P. M. Leitman ; L. G. Lohman ; L. C. Maia ; G. Martinelli ; for the license to carry out our fieldwork, and Daniel Reis, director of M. Memezes ; M. P. Morim ; M. A. Nadruz Coelho ; A. L. Peixoto ; Veadeiros National Park, for field work facilities. We thank the curators J. R. Pirani ; J. Prado ; L. P. Queiroz ; V. C. Souza ; J. R. Stehman ; of the following herbaria for kindly providing access to their collections: L. S. Sylvestre ; B. M. T. Wal . Rio de Janeiro : Andrea Jakobsson Estudio. CEN, HEPH, HMS, IBGE, NX, UB, UFG, R, RB, SP, and SPF. Finally, we Jardim Botânico do Rio de Janeiro . thank two reviewers for the excellent suggestions. Müller, K. and T. Borsch . 2005 . Phylogenetics of Utricularia (Lentibulariaceae) and molecular evolution of the trnK intron in a lineage with high sub- Literature Cited stitutional rates . Plant Systematics and Evolution 250: 39 – 67 . Munhoz, C. B. R. and J. M. Felfili . 2006 . Floristics of the herbaceous and sub- Bove, C. P . 2008 . A new species of Utricularia (Lentibulariaceae) from shrub layer of a moist grassland in the Cerrado biosphere reserve (Alto Central Brazil . Revista Brasileira de Botânica 31: 555 – 558 . Paraíso de Goiás), Brazil . Edinburgh Journal of Botany 63: 343 – 354 . Guisande, C., C. Granado-Lorencio , C. Andrade-Sossa , and S. R. Duque . Taylor, P . 1989 . The genus Utricularia – a taxonomic monograph . Kew 2007 . Bladderworts . Functional Plant Science and Biotechnology 1: Bulletin Additional Series 14: 1 – 724 . 58 – 68 . Thiers, B . [ 2010 and continuously updated]. Index Herbariorum: A global IUCN . 2001 . IUCN red list categories and criteria, version 3.1. IUCN, Gland, directory of public herbaria and associated staff . New York Botanical Switzerland & Cambridge : Information Press . Garden’s Virtual Herbarium . http://sweetgum.nybg.org/ih/ .